Abstract
Dendrites of many types of neurons contain voltage-dependent conductances that are active at subthreshold membrane potentials. To understand the computations neurons perform it is key to understand the role of active dendrites in the subthreshold processing of synaptic inputs. We examine systematically how active dendritic conductances affect the time course of postsynaptic potentials propagating along dendrites, and how they affect the interaction between such signals. Voltage-dependent currents can be classified into two types that have qualitatively different effects on subthreshold input responses: regenerative dendritic currents boost and broaden EPSPs, while restorative currents attenuate and narrow EPSPs. Importantly, the effects of active dendritic currents on EPSP shape increase as the EPSP travels along the dendrite. The effectiveness of active currents in modulating the EPSP shape is determined by their activation time constant: the faster it is, the stronger the effect on EPSP amplitude, while the largest effects on EPSP width occur when it is comparable to the membrane time constant. We finally demonstrate that the two current types can differentially improve precision and robustness of neural computations: restorative currents enhance coincidence detection of dendritic inputs, whereas direction selectivity to sequences of dendritic inputs is enhanced by regenerative dendritic currents.








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Agmon-Snir, H., Carr, C. E., & Rinzel, J. (1998). The role of dendrites in auditory coincidence detection. Nature, 393(6682), 268–272.
Angelo, K., London, M., Christensen, S. R., & Häusser, M. (2007). Local and global effects of I h distribution in dendrites of mammalian neurons. Journal of Neuroscience, 27(32), 8643–8653.
Bressloff, P. C. (1999). Resonantlike synchronization and bursting in a model of pulse-coupled neurons with active dendrites. Journal of Computational Neuroscience, 6(3), 237–249.
Chklovskii, D. B. (2004). Synaptic connectivity and neuronal morphology: Two sides of the same coin. Neuron, 43(5), 609–617.
Coombes, S., Timofeeva, Y., Svensson, C. M., Lord, G. J., Josić, K., Cox, S. J., et al. (2007). Branching dendrites with resonant membrane: A “sum-over-trips” approach. Biological Cybernetics, 97(2), 137–149.
Gillessen, T., & Alzheimer, C. (1997). Amplification of EPSPs by low Ni2 + - and amiloride-sensitive Ca2 + channels in apical dendrites of rat CA1 pyramidal neurons. Journal of Neurophysiology, 77(3), 1639–1643.
Goldberg, J. A., Deister, C. A., & Wilson, C. J. (2007). Response properties and synchronization of rhythmically firing dendritic neurons. Journal of Neurophysiology, 97(1), 208–219.
Hausselt, S. E., Euler, T., Detwiler, P. B., & Denk, W. (2007). A dendrite-autonomous mechanism for direction selectivity in retinal starburst amacrine cells. PLoS Biology, 5(7), e185.
Hines, M. L., & Carnevale, N. T. (1997). The neuron simulation environment. Neural Computation, 9(6), 1179–1209.
Hu, H., Martina, M., & Jonas, P. (2010). Dendritic mechanisms underlying rapid synaptic activation of fast-spiking hippocampal interneurons. Science, 327(5961), 52–58.
Hutcheon, B., & Yarom, Y. (2000). Resonance, oscillation and the intrinsic frequency preferences of neurons. Trends in Neurosciences, 23(5), 216–222.
Jack, J. J., & Redman, S. J. (1971a). An electrical description of the motoneurone, and its application to the analysis of synaptic potentials. Journal of Physiology, 215(2), 321–352.
Jack, J. J., & Redman, S. J. (1971b). The propagation of transient potentials in some linear cable structures. Journal of Physiology, 215(2), 283–320.
Jack, J. J., Miller, S., Porter, R., & Redman, S. J. (1971). The time course of minimal excitory post-synaptic potentials evoked in spinal motoneurones by group Ia afferent fibres. Journal of Physiology, 215(2), 353–380.
Joris, P. X., Smith, P. H., & Yin, T. C. (1998). Coincidence detection in the auditory system: 50 years after Jeffress. Neuron, 21(6), 1235–1238.
Koch, C. (1984). Cable theory in neurons with active, linearized membranes. Biological Cybernetics, 50(1), 15–33.
Lipowsky, R., Gillessen, T., & Alzheimer, C. (1996). Dendritic Na + channels amplify EPSPs in hippocampal CA1 pyramidal cells. Journal of Neurophysiology, 76(4), 2181–2191.
Livingstone, M. S. (1998). Mechanisms of direction selectivity in macaque V1. Neuron, 20(3), 509–526.
London, M., & Häusser, M. (2005). Dendritic computation. Annual Review of Neuroscience, 28, 503–532.
Magee, J. C. (1998). Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. Journal of Neuroscience, 18(19), 7613–7624.
Magee, J. C. (1999). Dendritic I h normalizes temporal summation in hippocampal CA1 neurons. Nature Neuroscience, 2(6), 508–514.
Mathews, P. J., Jercog, P. E., Rinzel, J., Scott, L. L., & Golding, N. L. (2010). Control of submillisecond synaptic timing in binaural coincidence detectors by Kv1 channels. Nature Neuroscience, 13(5), 601–609.
Mauro, A., Freeman, A. R., Cooley, J. W., & Cass, A. (1972). Propagated subthreshold oscillatory response and classical electrotonic response of squid giant axon. Biophysik, 8(2), 118–132.
Migliore, M., & Shepherd, G. M. (2002). Emerging rules for the distributions of active dendritic conductances. Nature Reviews Neuroscience, 3(5), 362–370.
Povysheva, N. V., Gonzalez-Burgos, G., Zaitsev, A. V., Kröner, S., Barrionuevo, G., Lewis, D. A., et al. (2006). Properties of excitatory synaptic responses in fast-spiking interneurons and pyramidal cells from monkey and rat prefrontal cortex. Cerebral Cortex, 16(4), 541–552.
Rall, W. (1964). Theoretical significance of dendritic trees for neuronal input–output relations. In R. F. Reiss (Ed.), Neural theory and modeling (pp. 122–146). Palo Alto: Stanford University Press.
Rall, W. (1967). Distinguishing theoretical synaptic potentials computed for different soma-dendritic distributions of synaptic input. Journal of Neurophysiology, 30(5), 1138–1168.
Rall, W., Burke, R. E., Smith, T. G., Nelson, P. G., & Frank, K. (1967). Dendritic location of synapses and possible mechanisms for the monosynaptic EPSP in motoneurons. Journal of Neurophysiology, 30(5), 1169–1193.
Remme, M. W. H., Lengyel, M., & Gutkin, B. S. (2009). The role of ongoing dendritic oscillations in single-neuron dynamics. PLoS Computational Biology, 5(9), e1000, 493.
Remme, M. W. H., Lengyel, M., & Gutkin, B. S. (2010). Democracy-independence trade-off in oscillating dendrites and its implications for grid cells. Neuron, 66(3), 429–437.
Sabah, N. H., & Leibovic, K. N. (1969). Subthreshold oscillatory responses of the Hodgkin-Huxley cable model for the squid giant axon. Biophysical Journal, 9(10), 1206–1222.
Schwartzkroin, P. A., & Slawsky, M. (1977). Probable calcium spikes in hippocampal neurons. Brain Research, 135(1), 157–161.
Schwindt, P. C., & Crill, W. E. (1995). Amplification of synaptic current by persistent sodium conductance in apical dendrite of neocortical neurons. Journal of Neurophysiology, 74(5), 2220–2224.
Scott, L. L., Mathews, P. J., & Golding, N. L. (2005). Posthearing developmental refinement of temporal processing in principal neurons of the medial superior olive. Journal of Neuroscience, 25(35), 7887–7895.
Scott, L. L., Mathews, P. J., & Golding, N. L. (2010). Perisomatic voltage-gated sodium channels actively maintain linear synaptic integration in principal neurons of the medial superior olive. Journal of Neuroscience, 30(6), 2039–2050.
Sirovich, L., & Knight, B. W. (1977). On subthreshold solutions of the Hodgkin–Huxley equations. Proceedings of the National Academy of Sciences of the United States of America, 74(12), 5199–5202.
Softky, W. (1994). Sub-millisecond coincidence detection in active dendritic trees. Neuroscience, 58(1), 13–41.
Stuart, G., Spruston, N., Sakmann, B., & Häusser, M. (1997). Action potential initiation and backpropagation in neurons of the mammalian CNS. Trends in Neurosciences, 20(3), 125–131.
Traub, R. D., Buhl, E. H., Gloveli, T., & Whittington, M. A. (2003). Fast rhythmic bursting can be induced in layer 2/3 cortical neurons by enhancing persistent Na + conductance or by blocking BK channels. Journal of Neurophysiology, 89(2), 909–921.
Tukker, J. J., Taylor, W. R., & Smith, R. G. (2004). Direction selectivity in a model of the starburst amacrine cell. Visual Neuroscience, 21(4), 611–625.
Williams, S. R., & Stuart, G. J. (2000). Site independence of EPSP time course is mediated by dendritic I h in neocortical pyramidal neurons. Journal of Neurophysiology, 83(5), 3177–3182.
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This work was supported by a grant from the US National Institutes of Health: DC008543 to JR.
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Remme, M.W.H., Rinzel, J. Role of active dendritic conductances in subthreshold input integration. J Comput Neurosci 31, 13–30 (2011). https://doi.org/10.1007/s10827-010-0295-7
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DOI: https://doi.org/10.1007/s10827-010-0295-7